Genes, copying, and female mate choice: shifting thresholds

Recent experimental work on guppies (Poecilia reticulata) hasexamined the strength of genetic and cultural (copying) factorsin determining female mate choice. Using females from a populationwith a heritable preference for the amount of orange body colorpossessed by males, prior work discovered that a threshold differencein orange color among males existed below which females wouldchoose a less orange male if they observed another female choosethat male, but above which they consistently preferred the moreorange of the males, regardless of whether they viewed anotherfemale prefer the less orange male. I tested whether this thresholdcan be shifted by increasing the amount of mate-copying informationavailable to a female. I demonstrate that when a female hasthe opportunity to see two different model females independentlyprefer the less orange of two males or a single female neara drab male for a longer period of time (twice as long as inprior work), the observer female prefers this drab male evenwhen males dramatically differ in orange coloration.     

Learned mate recognition and reproductive isolation in guppies

Research on learned species discrimination has focused on the consequences of early experience. However, in species where parental care is limited or absent, including most fish, juveniles have fewer opportunities to learn from adult conspecifics. We examined male mate recognition in Trinidadian guppies, Poecilia reticulata, and in their sister species, the swamp guppy, P. picta. Choice tests revealed that males from localities where their species is the only poeciliid present initially mated with conspecific and heterospecific females at random. In contrast, P. reticulata and P. picta found in sympatry preferred their own females. We then investigated the acquisition of mating discrimination by wild P. reticulata males from two allopatric populations. Males that were allowed to interact with females of both species learned within 4 days to distinguish conspecific partners, and within a week their species discrimination matched that of sympatric populations. This study confirms that learning is important in the acquisition of adult mating preferences and shows why learned mate preferences can be important in the last stages of speciation.     

Mate Preference for Novel Phenotypes: A Fresh Face Matters

Conspicuous polymorphism in sexually selected traits is usually attributed to processes such as frequency‐dependent selection that can maintain genetic variation. Recent evidence indicates that dramatic variation of male coloration in guppies (Poecilia reticulata) is promoted by a form of frequency‐dependent selection in which males bearing rare or novel color patterns achieve higher mating success than males bearing common patterns. Active female preference for unfamiliar or rare color patterns has been implicated in generating this rare‐phenotype advantage, but the behavioral processes responsible for the preference remain unclear. To determine whether familiarity that is developed over a very short timescale can lead to a rare‐male mating advantage, we measured female response to courtship by males with color patterns that were the same as or different from that of the previous male to court. Females showed two types of short‐term preference variation in this experiment. On the first trial day, females shifted their preferences on a timescale of minutes, showing strong preference for males bearing a color pattern different from that of the immediately previous male to court. Twenty‐four hours later, females were less responsive to male courtship overall, and there was no difference in females’ response to different‐ and same‐morph males. Females also preferred males with more orange coloration on both trial days, but this color preference was independent of the preference for ‘different’ color patterns. These data suggest that the behavioral process underlying rare‐male advantage in guppies is that females prefer males bearing unfamiliar color patterns and that familiarity is determined over a very short timescale.     

Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae

Variation in mating preferences coupled with selective predation may allow for the maintenance of alternative mating strategies. Males of the South American live‐bearing fish Poecilia parae fall in one of five discrete morphs: red, yellow, blue, stripe‐coloured tail (parae) and female mimic (immaculata). Field surveys indicate that the red and yellow morphs are the rarest and that their rarity is consistent across years. We explored the role of variable female mating preference and selective predation by visual predators in explaining the rarity of red and yellow males, and more generally, the maintenance of this extreme colour polymorphism. We presented wild‐caught P. parae females and Aequidens tetramerus, the most common cichlid predator, with the five male colour morphs in separate trials to determine mating and prey preferences, respectively. We found that a large proportion of females shared a strong preference for the rare carotenoid‐based red and yellow males, but a distinct group also preferred the blue and parae morphs. The cichlid predator strongly preferred red and yellow males as prey. Together, these results suggest that the interaction between premating sexual selection favouring and predation acting against the red and yellow morphs may explain their rarity in the wild. The trade‐off between sexual and natural selection, accompanied by variation in female mating preferences, may therefore facilitate the maintenance of the striking colour polymorphism in P. parae.     

Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

Sexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.     

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Genetic difference in female choice between two guppy populations

The pattern of mating preferences of female guppies, Poecilia reticulata, differs genetically between two Trinidadian populations. Males from the Aripo and Paria rivers of Trinidad differ in the extent and intensity of orange pigment in their colour patterns. The relative area of orange in Paria colour patterns was nearly twice that in Aripo colour patterns. To test the hypothesis that a difference in female mating preferences could have contributed to the difference in colour patterns, patterns of female choice between laboratory-reared Paria and Aripo females were compared. The frequency of sexual responses to male courtship displays was used to measure the average preference of females for individual males. Paria females discriminated significantly between Paria males based upon differences in the extent of orange in the colour pattern. Aripo females showed no evidence of discrimination between Paria males, and thus differed significantly from Paria females in choice behaviour. Neither group of females discriminated between Aripo males. These results are evidence that female choice behaviour can vary genetically within a species and suggest that differences in preferences may have contributed to divergence in colour patterns among guppy populations.     

Change in male coloration associated with artificial selection on foraging colour preference

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour‐based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour‐based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour‐based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.     

Female mate preference based on male orange spot patterns in the feral guppy <Emphasis Type="Italic">Poecilia reticulata</Emphasis> in Japan

It is known that females prefer males with larger and/or brighter orange spots in many populations of the guppy Poecilia reticulata. However, female preference for male orange spots varies among populations and changes within several years when they are introduced into new habitats with different environment. Guppies were introduced into Okinawa, Japan, more than 20 years ago and were subjected to natural and sexual selection for a long period. The female preference for orange spot patterns of males was examined by the dichotomous choice experiment for a feral guppy population of the Hiji River, Okinawa. We chose full-sibling males as a pair of stimulus males that were simultaneously presented to a test female, because sibling males should resemble each other. To create different orange spot patterns between stimulus males, one male of the stimulus male pair was fed carotenoid-supplement food such as algae and another male was fed low-carotenoid food. High-carotenoid-treatment males showed not only brighter coloration of orange spots but also larger spots than other males as a result of this dietary-manipulation. In the dichotomous choice experiment, females preferred the high-carotenoid-treatment males. In addition, logistic regression analysis clarified that brighter coloration of male orange spots was the most important factor for female mate preference. This finding suggests indirect benefits of female preference for male orange spot patterns if the male foraging ability for algae were heritable.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Intrasexual competition facilitates the evolution of alternative mating strategies in a colour polymorphic fish

Background  

Intense competition for access to females can lead to males exploiting different components of sexual selection, and result in the evolution of alternative mating strategies (AMSs). Males of Poecilia parae, a colour polymorphic fish, exhibit five distinct phenotypes: drab-coloured (immaculata), striped (parae), structural-coloured (blue) and carotenoid-based red and yellow morphs. Previous work indicates that immaculata males employ a sneaker strategy, whereas the red and yellow morphs exploit female preferences for carotenoid-based colours. Mating strategies favouring the maintenance of the other morphs remain to be determined. Here, we report the role of agonistic male-male interactions in influencing female mating preferences and male mating success, and in facilitating the evolution of AMSs.     

GEOGRAPHIC VARIATION IN FEMALE PREFERENCES FOR MALE TRAITS IN POECILIA RETICULATA

We examined the preferences of female guppies (Poecilia reticulata) from 11 localities in Trinidad with respect to male color-pattern elements, body shape and size, and overall color and brightness contrast. Females are on average more attracted to males from their own population than from alien populations, and populations appear to vary in the criteria used in female choice. Multiple-regression analysis suggests that mate-preference criteria vary among localities in intensity, sign, and the number of traits used. Although preference estimators and color-pattern parameters are unique to each population, only orange, black, and color contrast showed a correlation between degree of male trait and degree of preference for that trait. There is a clear effect of water color and a possible effect of predation intensity. The results are discussed in light of various models of sexual selection and the early stages of speciation.     

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids

Female mating preference based on male nuptial coloration hasbeen suggested to be an important source of diversifying selectionin the radiation of Lake Victoria cichlid fish. Initial variationin female preference is a prerequisite for diversifying selection;however, it is rarely studied in natural populations. In clearwater areas of Lake Victoria, the sibling species Pundamiliapundamilia with blue males and Pundamilia nyererei with redmales coexist, intermediate phenotypes are rare, and most femaleshave species-assortative mating preferences. Here, we studya population of Pundamilia that inhabits turbid water wheremale coloration is variable from reddish to blue with most malesintermediate. We investigated male phenotype distribution andfemale mating preferences. Male phenotype was unimodally distributedwith a mode on intermediate color in 1 year and more blue-shiftedin 2 other years. In mate choice experiments with females ofthe turbid water population and males from a clearer water population,we found females with a significant and consistent preferencefor P. pundamilia (blue) males, females with such preferencesfor P. nyererei (red) males, and many females without a preference.Hence, female mating preferences in this population could causedisruptive selection on male coloration that is probably constrainedby the low signal transduction of the turbid water environment.We suggest that if environmental signal transduction was improvedand the preference/color polymorphism was stabilized by negativefrequency-dependent selection, divergent sexual selection mightseparate the 2 morphs into reproductively isolated species resemblingthe clear water species P. pundamilia and P. nyererei.     

The relative importance of orange spot coloration and total length of males in female guppy mate preference

Female mate choice by multiple male traits is an important current topic in animal behavior. However, the relative importance among the multiple cues in female choice is not explored in most cases. Female guppies Poecilia reticulata use both the color saturation of orange spots and the total length of males as mate choice criteria. In the present study, we used digitally modified video playbacks to examine the relative importance of these two male traits to female mate preferences. We initially examined the effective difference in the color saturation of orange spots as well as that in total length between two stimulus male images. Females only showed a strong preference for a bright male image (compared to the dull image) when the difference in color saturation was large (91% versus 25%). Conversely, females only exhibited a preference for larger size when they were presented a choice between two relatively small male images (total length 26.0 mm versus 23.0 mm). When two male images in which both the two traits were modified were presented to females, they prioritized male images possessing higher color saturation of orange spots, indicating the color saturation of male orange spots to be a more important factor than the total length in their mate choice. The color saturation of orange spots may convey more reliable information about the males to the females than their total lengths. These findings imply that females may rank multiple male criteria depending on relative benefits or costs derived from their mate choice based on each criterion.     

No evidence for color or size preference in either sex of a dichromatic stream fish, Percina roanoka

Sexual dimorphism is hypothesized to be the result of differential selection pressures between the sexes. Dimorphic traits can serve as indicators of mate quality, altering mate preferences in the opposite sex in favor of a conspicuous trait. Common indicators of mate quality include color and size, with traditional assumptions and evidence predicting a preference for more colorful and/or larger sized mates in many species. Both male and female preferences for more colorful and larger mates within a species are rarely examined simultaneously, however. We examined a sexually dichromatic freshwater fish, Percina roanoka and found that male coloration is positively correlated with size, suggesting color may function as an indicator of viability. We tested preferences for coloration and size in both sexes in a dichotomous mate choice setup in which only visual signals were exchanged. Neither females nor males exhibited a color or size preference in individuals of the opposite sex. Visual cues alone therefore appear to be insufficient to elicit a significant preference in both sexes of this species. Male coloration in P. roanoka does not appear to be driven solely by female preference.     

Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration

This study evaluated whether diversity in male ornamental traits between populations is associated with a corresponding diversity in female preferences, or whether males can evolve divergent ornamentation even when female preferences remain relatively consistent. Video editing techniques were used to manipulate the coloration of recorded images of male three-spined sticklebacks, Gasterosteus aculeatus, and these images were presented to female sticklebacks from populations with black or red male nuptial coloration. Overall, females responded preferentially to images of males with black or red coloration over images with the dull coloration of females and some males; although preferences differed between populations, these differences were not statistically significant. Thus divergence in male ornaments was probably not caused by a corresponding divergence in female preferences. The results do not, however, allow clear discrimination between the various hypotheses for the evolution of female mating preferences.     

Use of digitally modified videos to examine female mate preference for orange spot coloration of males in the guppy, Poecilia reticulata

Digitally modified video techniques may provide some advantages for the behavioral study of animals, including fishes. However, the validity of the experiments that are conducted using digitally modified videos should be verified. In the present study, we examined female mate preference in the guppy, Poecilia reticulata in a Japanese population by exploring an appropriate method involving the use of digitally modified video playbacks. For the male stimulus, two video images were produced by digital modification of a video recording of a male; the brightness of the orange spot coloration of the male was enhanced (bright male) in one video and decreased (dull male) in the other video. In experiment 1, female choice was examined according to the method described in previous studies, i.e., two monitors were set on opposite sides of the test aquarium to simultaneously present two stimulus male images to the females. However, in this experiment, the stimulus male images did not attract the females to a greater extent than the blank aquarium images. In addition, although the first trial showed a female preference for bright males, in the second trial, in which each stimulus male image was shown from the monitor opposite to that used in the first trial, a significant preference for bright males could not be detected. In experiment 2, a monitor was placed on one side of the aquarium and the left and right sides of the monitor showed the two stimulus male images simultaneously. In addition, a 24-h time interval was set between the first and second trials. Females spent more time in the proximity of the male images than that of the blank images, and a female preference for bright males was observed in both trials. The results of this study clearly indicate the female preference for males possessing bright coloration of orange spots. These results also suggest that the one-sided monitor system adopted in experiment 2 is a more appropriate method than the two-sided monitor system to examine female mate preferences by using digitally modified video playbacks.